Invest Clin 63(2): 137 - 146, 2022 https://doi.org/10.54817/IC.v63n2a03
Corresponding Author. Mauricio Pierdant Pérez, Av. Venustiano Carranza 2405, Colonia Los Filtros, Código Postal
78394, San Luis Potosí, SLP, México. E-mail: mpierdant@hotmail.com
Changes in chloremia, secondary to hydric
reanimation during the first 24 hours,
increases hospital stay and complications
in patients with acute pancreatitis.
Rafael Silva Olvera1, Mauricio Pierdant Pérez2, Gustavo Ibarra Cabañas1, Iván Ledezma
Bautista2, Raúl Alejandro Hernández Rocha2 and Antonio Augusto Gordillo Moscoso2
1 Instituto Mexicano del Seguro Social. Hospital General Zona No. 50, San Luis Potosí,
SLP, México
2 Facultad de Medicina, Universidad Autónoma de San Luis Potosí, Departamento
de Salud Pública y Ciencias Médicas, San Luis Potosí, SLP, México.
Key words: Pancreatitis; chlorides; isotonic solutions; length of stay.
Abstract. Acute pancreatitis (AP) requires first-line treatment with in-
tensive fluid resuscitation. Hydroelectrolyte changes secondary to this man-
agement could be related to an increase in hospital stay, complications, and
mortality. The objective of this study was to correlate the increase in serum
chlorine (> 8mEq / L) during the first 24 hours (ISC) with a longer hospital
stay, complications and mortality in patients with AP. A total of 110 patients
with AP admitted to the emergency room were included. Fluid management
and serum chlorine were recorded on admission and after 24 hours; duration
of hospital stay, complications and mortality, were also registered. 37 patients
had ISC (age 56.4 ± 18.4 years; 51% women), there were no differences in age,
sex or type of fluid management with patients without ISC. In bivariate analysis,
ISC was associated with severe AP (30% vs 12%, p = 0.02), higher APACHE II
score at admission (8 [6-15] vs 6 [4-9] points, p = 0.006), and longer hospital
stay (9 [7-12] vs 7 [5-10] days, p = 0.03). The overall mortality and compli-
cations rate were 16% and 25%, respectively, with no differences between the
groups (24% vs. 12%, p = 0.1 and 35% vs. 19%, p = 0.06). After multivariate
adjustment, independent predictors of hospital stay were ISC> 8 mEq / L (p
= 0.01) and APACHE II scores at 24 hours (p = 0.02). We conclude that ISC is
associated with a longer hospital stay in patients with AP from a second-level
hospital care population.
138 Silva Olvera et al.
Investigación Clínica 63(2): 2022
Cambios en la cloremia secundaria a la reanimación hídrica,
en las primeras 24 horas, incrementa la estancia hospitalaria
y las complicaciones en los pacientes con pancreatitis aguda.
Invest Clin 2022; 63 (2): 137 – 146
Palabras clave: pancreatitis; cloruros; soluciones isotónicas; tiempo de internación.
Resumen. La pancreatitis aguda (PA) requiere tratamiento de primera
línea con reanimación hídrica intensiva. Los cambios hidroelectrolíticos se-
cundarios a este manejo podrían relacionarse a un incremento en la estancia
hospitalaria, complicaciones y mortalidad. El objetivo de este estudio fue corre-
lacionar el incremento de cloro sérico (>8mEq/L) en las primeras 24hrs (ICS),
con una mayor estancia hospitalaria, complicaciones y mortalidad en pacientes
con PA. Se incluyeron 110 pacientes con PA ingresados a urgencias, se registró
el manejo hídrico y cloro sérico al ingreso y 24 horas después, la estancia hos-
pitalaria, complicaciones y mortalidad. 37 pacientes tuvieron ICS (edad 56,4
± 18,4 años; 51% mujeres) no hubo diferencias en edad, sexo o tipo de manejo
hídrico en pacientes sin ISC. En el análisis bivariado, el ICS se asoció a PA grave
(30% vs 12%, p = 0,02), mayor puntuación APACHE II al ingreso (8 [6-15] vs
6 [4-9] puntos, p = 0,006) y estancia hospitalaria más prolongada (9 [7-12]
frente a 7 [5-10] días, p = 0,03). La tasa global de mortalidad y complicaciones
fueron del 16% y el 25%, respectivamente, sin diferencias entre grupos (24%
vs 12%, p = 0,1 y 35% vs 19%, p = 0,06). Después del ajuste multivariado, los
predictores independientes de la estancia hospitalaria fueron ICS> 8 mEq/L (p
= 0,01) y las puntuaciones APACHE II a las 24 horas (p = 0,02). Concluimos
que el ICS se asocia a mayor estancia hospitalaria en pacientes con PA de una
población de segundo nivel de atención hospitalaria.
Received: 19-07-2021 Accepted: 24-02-2022
INTRODUCTION
Acute Pancreatitis (AP) is an inflam-
matory disease that frequently involves peri-
pancreatic tissue and can englobe distant
organs and systems 1,2. The incidence var-
ies between 4.9 and 73.4 cases per 100,000
people in the world 3. Its etiology is mainly
attributed to biliary lithiasis and alcoholism,
and between 10 and 30% is classified as idio-
pathic 1. There are prognostic factors of mor-
tality, like the Ranson, Glasgow-Imrie, POP,
BISAP criteria, and Hong Kong scale that is
based in glycemia-urea and gives a prognosis
with adequate accuracy 4.
Initial management of AP is based in
hydric reanimation with intravenous liquids,
mainly isotonic solutions, such as saline
solution 0.9% (SS0.9%) and Ringer lactate
(RL), and pain control 1,2,5.
The recommendation is to administer
balanced solutions in a range of 200 to 500
milliliters per hour or 5 to 10 mL per kg of
weight per hour, with a range of 2,500 and
4,000 mL in 24 hours. There are few studies
to support the decision of what type of solu-
tion to administer 1. A meta-analysis showed
no statistically significant differences in the
incidence of necrotizing PA comparing the
use of SS0.9% or RL 6.
Chloremia changes due to hydric reanimation and complications in pancreatitis 139
Vol. 63(2): 137 - 146, 2022
Retrospective studies suggest that ag-
gressive administration of fluids in the ini-
tial 12-24 hours reduces morbi-mortality 1.
Being that the SS0.9% is used globally as
the first line of therapy despite having an
osmolarity of 308, and a pH 5.5, and supra
physiologic concentrations of sodium and
chloride, and that could increase patient
morbi-mortality 7.
Chloride (Cl-) is the main anion of hu-
man body, with functions maintaining oncot-
ic pressure, acid-base equilibrium, muscular
activity, osmosis, and immunomodulation.
The SS0.9% could induce pathologic
hyperchloremia (Table 1) and hyperchlore-
mic metabolic acidosis 8. In intensive care
units, hyperchloremia was associated as an
independent factor of mortality in major
trauma 9, acute kidney injury 10 and systemic
inflammatory response syndrome 8,11.
Metabolic hyperchloremic acidosis in
experimental studies with septic animals has
demonstrated that it increases the produc-
tion of interleukin 6, tumor necrosis factor,
and nitric oxide; thus hyperchloremia is a
pro-inflammatory modulator in sepsis 4,11.
In accordance to Kumpers et al, an in-
fusion of two liters of SS0.9% reduces 12%
of the blood supply in the renal cortex of
healthy patients, as demonstrated with an-
giography 12. The hyperchloremia, according
to Marttinen et al., associates with the risk
of acute kidney injury, secondary to vaso-
constriction of the afferent renal artery 10,
decreasing the glomerular filtration rate,
which leads to that exposed patients to non-
guided chloride management, require more
replacement therapy 13.
Associated mortality with hyperchlore-
mia is between 30-40%, with concentrations
Table 1
Causes of hyperchloremia.
Pseudohiperchloremia Loss of water and electrolytes
- High concentrations of solids in serum
(fatty acids or proteins), dilutional
- Bromide or iodide intoxication
- Certain forms of diarrhea
- Osmotic diuresis
- Certain cases of post-obstructive diuresis
Administration of fluids with
high chloride containing Associated with metabolic acidosis
- Saline Solution 0.9%
- Albumin
- Ammonium Chloride
- Parenteral nutrition
- Certain forms of diarrhea
- Tubular renal acidosis
- Inhibitors of carbonic anhydrase
- Ureteral deviation (for example, ileal bladder).
- Administration of ammonium chloride.
- Administration of arginine chlorhidrate,
hydrochloric acid, or lysine.
-Certain cases of chronic kidney disease.
Organic acidosis with fast excretion of acid anion
(for example: toluene overdose).
Net loss of water Respiratory alkalosis
- Exercise
- Severe dehydration
- Fever
- Hypermetabolic status
- Insipidus diabetes
140 Silva Olvera et al.
Investigación Clínica 63(2): 2022
of chloremia higher of 130mEq/L, having
basal chloride levels of 80 and 120mEq/L
in patients with systemic inflammatory re-
sponse syndrome, demonstrating that the
greater input of intravenous solutions, the
greater hospital mortality 8.
In major trauma it was associated with
30-days mortality, analyzing chloremia at
admission and 48 hours later, showing and
elevation of serum levels in non-surviving
patients, compared with survivors, with a
chloride delta (ΔCl, that is the difference
between chloremia at admission minus 48
hours chloremia) higher in the non-survivors
(ΔCl 10.3±11.1mmol/L vs 1.7±5.2mmol/L,
p<0.001). The administration of less than
1,500ml SS0.9% was not associated with
mortality 9 and it has a limit of maximum 1
Liter in 24 hours 14.
The aim of this study was to correlate
a significant increment of chloremia during
the first 24 hours in patients with acute pan-
creatitis, with hospital stay and mortality of
any cause, and to describe the presence of
complications.
PATIENTS AND METHODS
Study design and patients
The present study was reviewed and ap-
proved by IMSS scientific and ethics com-
mittees with the number R-2017-2402-39
and was made with a database of IMSS Zone
50 Hospital registry, San Luis Potosi, Mexi-
co. This database processed the registry of
all consecutive admitted adults in the emer-
gency room between January 2015 and De-
cember 2016, with diagnosis of acute pan-
creatitis. It includes demographic data and
clinical information, medical procedures,
etiology of pancreatitis, and subsequent
laboratory findings. The data are periodi-
cally integrated, reviewed, and checked for
accuracy.
For this retrospective, observational and
analytic study, data from all patients admit-
ted in the mentioned period was examined.
We included patients who met the following
criteria: (i) diagnosis of acute pancreatitis
based in clinical characteristics, radiologic
findings and pancreatic inflammation mark-
ers, following the 2012 Atlanta criteria revi-
sion, (ii) had serum basal electrolytes at ad-
mission and 24 hours later, (iii) underwent
hospitalization without volunteer discharge.
We excluded patients: (i) referred from oth-
er medical units with diagnosis of acute pan-
creatitis that received previous initial man-
agement, (ii) patients that had treatment
with drugs that could affect chloremia, such
as thiazides, diuretics, potassium-sparring
diuretics, etc., and (iii) patients that had a
disease that affected their renal function.
Outcome
The primary outcome of this study was
hospital stay (measured in days); mortality
for any cause, besides the presence of re-
gional complications, such as peri-pancreat-
ic collection, pancreatic and peri-pancreatic
necrosis, gastric juice secretion, splenic in-
farct, colonic necrosis, pseudoaneurisms,
splenic and portal vein thrombosis, and
pancreatic ascites. Besides systemic compli-
cations defined as preexisting comorbidity
exacerbation; coronary disease, pulmonary
chronic disease, were registered and ana-
lyzed in the same complications category.
Laboratory procedures
The chloremia measures at admission
and after 24 hours, was performed with in-
direct potentiometry (cobas c 501 analyzer,
Roche Diagnostics, Indianapolis, IN, USA)
and the results were expressed in milliequiv-
alents per liter (mEq/L). We define ISC as
the increment of >8 mEq/L through the
first 24 hours, according to our observation
in clinical practice and results of the data
base.
Statistical analysis
Data distribution was assessed using the
Shapiro-Wilk test. Continuous variables were
expressed as mean ± standard deviation for
normal distribution, and as median [inter-
Chloremia changes due to hydric reanimation and complications in pancreatitis 141
Vol. 63(2): 137 - 146, 2022
quartile range] for non-normal distribution,
while categorical variables were described
as percentages and proportions. To evalu-
ate differences, we used Student’s t test/U-
Mann Whitney test, and Chi-square/Fisher
exact test, as appropriated. The primary out-
come was the hospital stay in days, defined
as the period between their emergency room
admission and medical discharge; due to im-
provement or death (we excluded transferred
patients and voluntary discharges). The
chloremia delta was defined as chloremia af-
ter 24 hours minus chloremia at admission,
expressed in mEq/L. Multivariate analysis
was performed with multiple regression to
determine the role of different variables with
hospital stay in days. To estimate the power,
we used post-study power-test with the pwr
function, setting the significance in 0.05.
All analyses were two-tailed and a P value of
<0.05 was set for significance. R Studio ver-
sion 3.4.1 statistical software was used for
data analysis.
RESULTS
One hundred and ten patients were se-
lected for the analysis, its baseline and clinic
characteristics are shown in Table 2.
At 24 hours, 37 (33%) patients were
classified with an ISC (ΔCl>8mEq/L). There
were no differences in baseline character-
istics (age, sex and pancreatitis etiology)
between the two groups (ΔCl>8mEq/L,
ΔCl<8mEq/L). (Table 3).
Table 2
Descriptive statistical. Baseline and clinical characteristics of the population.
N=110 (%) Median [Q1-Q3] Mean ± SD
Age (years) 56 [42.2-69.7] 55.9±17.7
Sex (women) 63 (57)
Etiology
- Biliary
- Alcoholic
- Triglycerides
- Drugs
- Idiopathic
- Others
75 (68)
9 (8)
15 (14)
1 (1)
7 (6)
3 (3)
Severity
- Mild
- Moderate
- Severe
78 (71)
12 (11)
20 (18)
Chloremia at admission (mEq/L) 96.1 [93.5-99] 55.9±5.6
Admission APACHE II score 6 [4-7.7] 7.8±5.8
Used solution
- SS0.9%
- Hartmann
- SS0.9%>Hartmann
- Hartmann>SS0.9%
- Others
58 (53)
13 (12)
24 (22)
14 (13)
1 (1)
Quantity used (L) 4 [3.5-4.5] 4.06 ± 0.99
%: Percentage, Q1-Q3: Quartile 1 (P25) – Quartile 3 (P75), SD: Standard Deviation, h: hours, mEq/L: milliequi-
valents per liter, APACHE II: score of Acute Physiology and Chronic Health Evaluation II, SS0.9%: Saline Solution
0.9%, L: Liters.
142 Silva Olvera et al.
Investigación Clínica 63(2): 2022
Table 3
Bivariate analysis between increase in serum chlorine in 24 hours
ΔCl ≤8mEq/L vs ΔCl>8mEq/L.
N=110 (%) ΔCl ≤8mEq/L
N=73 (%)
ΔCl >8mEq/L
N=37 (%) p
Age (years)
Median [Q1-Q3]
Mean ± SD
56 [42.2-69.7]
55.9 ± 17.7
56 [43-69]
55.6 ± 4.7
56 [42-71]
56.4 ± 18.4 0.81ᵁ
Sex (women) 63 (57) 44 (60) 19 (51) 0.37ᵡ
Etiology
- Biliary
- Alcoholic
- Triglycerides
- Drugs
- Idiopathic
- Others
75 (68)
9 (8)
15 (14)
1 (1)
7 (6)
3 (3)
47 (64)
5 (15)
11 (15)
1 (1)
6 (8)
3 (4)
28 (75)
4 (11)
4 (11)
0
1 (3)
0
0.6ⅎ
Severity
- Mild
- Moderate
- Severe
78 (71)
12 (11)
20 (18)
58 (79)
6 (8)
9 (12)
20 (54)
6 (16)
11 (30)
0.02ᵡ
Chloremia at admission (mEq/L)
Median [Q1-Q3]
Mean ± SD
96.1 [93.5-99]
55.9 ± 5.6
97 [94.5-100]
97.1 ± 4.7
96 [92-97.5]
94.1 ± 6.6 0.03ᵁ
Chloremia after 24 h (mEq/L)
Median [Q1-Q3]
Mean ± SD
103 [99.2-106]
102.9 ± 5.4
102 [99-104.2]
101.9 ± 5.1
105 [103.8-108]
105.1 ± 5.6 0.0002ᵁ
Admission APACHE II (points)
Median [Q1-Q3]
Mean ± SD
6 [4-7.7]
7.8 ± 5.8
6 [4-9]
6.5 ± 4.5
8 [6-15]
10.2 ± 7.2 0.006ᵁ
24 hours APACHE II (points)
Median [Q1-Q3]
Mean ± SD
5 [3-7.3]
7.3 ± 7.4
5 [3-7]
6.3 ± 6.4
6 [4-13]
9.4 ± 8.8 0.13ᵁ
Hospital Stay (days)
Median [Q1-Q3]
Mean ± SD
8 [6-9.5]
9.5 ± 6.9
7 [5-10]
8.1 ± 4.2
9 [7-12]
12.3 ± 9.9 0.03ᵁ
Surgery
- Elective
- Urgency
- Not surgery performed
- Not needed
18 (16)
1 (1)
60 (55)
31 (28)
11 (15)
0
38 (52)
24 (32)
7 (19)
1 (3)
22 (59)
7 (19)
0.22ⅎ
Complications 27 (25) 14 (19) 13 (35) 0.06ᵡ
Mortality 18 (16) 9 (12) 9 (24) 0.10ᵡ
Chloremia changes due to hydric reanimation and complications in pancreatitis 143
Vol. 63(2): 137 - 146, 2022
Pancreatitis severity was stablished us-
ing the Atlanta criteria, and found as severe
in the 30% of all patients with ΔCl>8mEq/L,
compared with 12% of the patients with
chloremia delta ≤8mEq/L (p=0.02). There
were no differences in surgery indication in
both groups.
Considering the clinical results, ad-
mission APACHE II score was higher in the
group with ΔCl>8mEq/L (8 [6-15] vs 6 [4-
9] points, p=0.006), but had no differences
in APACHE II score 24 hours after (5 [3-7]
vs 6 [4-13] points, p=0.13).
Hospital stay was longer in the group
with ΔCl>8mEq/L (9 [7-12] vs 7 [5-10]
days, p=0.03). The power (β) of this assev-
eration is 0.99 with a significance level (α)
of 0.05.
There were not statistically significant
differences in complications (35% vs 19%,
p=0.06) and mortality (24% vs 12%, p=0.1).
Regarding the quantity of utilized solu-
tion in the first 24 hours from admission, we
found that in the ΔCl>8mEq/L the median
volume used was 4.25 [3.6-5] vs 3.9 [3.5-4.3]
liters in the ΔCl≤8mEq/L group (p=0.04).
The Table 3 summarize the bivariated
analysis of baseline and clinical outcomes of
the patients, divided following their chlor-
emia change.
In multivariate analysis modeling hospi-
talization days, final model was obtained with
step-wise regression using backward variable
elimination, showed that a ΔCl>8mEq/L
(p=0.01) and 24 hours APACHE II score
(p=0.02) stayed as the main predictors for
longer hospital stay in patients with acute
pancreatitis.
DISCUSSION
In this retrospective study of 110 pa-
tients with acute pancreatitis, we found
that the significant chloremia increment
in 24 hours (ΔCl>8mEq/L) could be an in-
dependent associated factor to prolong the
hospital stay in the adult population. Chlor-
emia concentration reflects patient’s elec-
trolyte and water balance; its change is at-
tributed fundamentally to the management
with crystalloid solutions. Thus, chloremia
changes are intimately related with the
kind and quantity of utilized solutions. Hy-
perchloremia at the same time is related
with the acid-base equilibrium. In fact, the
chloremia concentration increment is one
of three causes of metabolic acidosis, which
in animal studies increases the production
of interleukin 6 and tumoral necrosis fac-
tor, as well as nitric oxide, therefore, chlo-
N=110 (%) ΔCl ≤8mEq/L
N=73 (%)
ΔCl >8mEq/L
N=37 (%) p
Utilized solution
- SS0.9%
- Hartmann
- SS0.9%>Hartmann
- Hartmann>SS0.9%
- Others
58 (53)
13 (12)
24 (22)
14 (13)
1 (1)
34 (47)
12 (16)
15 (21)
11 (15)
1 (1)
24 (65)
1 (3)
9 (24)
3 (8)
0
0.08ᵡ
Quantity utilized (L)
Median [Q1-Q3]
Mean ± SD
4 [3.5-4.5]
4.06 ± 0.99
3.9 [3.5-4.3]
3.94 ± 0.86
4.25 [3.6-5]
4.31 ± 1.18 0.04ᵁ
%: Percentage, Q1-Q3: Quartile 1 (P25) – Quartile 3 (P75), SD: Standard Deviation, mEq/L: milliequivalents per
liter, APACHE II: score of Acute Physiology and Chronic Health Evaluation II scale, SS0.9%: Saline Solution 0.9%, L:
Liters. ᵡ: Chi-Square test, ⅎ: Exact Fisher Test, ᵁ: U-Mann-Whitney test, ᵀ: T-Student test.
Table 3. CONTINUACIÓN
144 Silva Olvera et al.
Investigación Clínica 63(2): 2022
ride is a pro-inflammatory modulator 11. It
has been found that this ion is important in
neutrophil functions, which requires con-
stant influx through the chloride channels
to produce hypochlorous acid from myelo-
peroxidase. For this reason, low extracel-
lular chloride concentration is associated
with neutrophil disfunction. This could pro-
vide a plausible pathophysiological link be-
tween the increment of chloremia and pro-
inflammatory state and longer hospital stay
in patients with acute pancreatitis. Recent
studies in cells and animals indicate that
hyperchloremic acidosis, through the in-
crement of hydrochloric acid, significantly
increases cytokines expression, besides the
gene induction through κB nuclear factor
and DNA junction. This seems to be espe-
cially relevant in states with important in-
flammatory response such as acute pancre-
atitis 11.
Previous studies had stablished the as-
sociation between hyperchloremia and in-
creased mortality in critically ill patients
8,9,11. Isolated hyperchloremia has been rec-
ognized as an independent factor associat-
ed with acute kidney injury 10. In our study,
although it did not reach statistical signifi-
cance, maybe because of the sample size, we
can see a trend in the increment of mortal-
ity with significant changes in chloremia, as
well as in the incidence of complications.
Nevertheless, there is still controversy that
chloremia changes are a consequence of ag-
gressive fluid therapy in patients with de-
plored hydration level, or if they truly are the
cause of mortality trough the inflammatory
mechanisms mentioned before. Controlled
prospective studies are needed to answer
this question.
Regarding the use of solutions, Fors-
mark et al recommend administration of a
range of 2.5 to 4 L in 24 hours; however,
in our population the average was 4.07 ±
0.99 L, even reaching 7.2 L in the first 24
hours. Although recommendation is the use
of crystalloids, either saline solution 0.9% or
Hartmann solution, there is still no consen-
sus as to which solution to use, although it
has been seen that Ringer lactate may be as-
sociated with an anti-inflammatory effect 1.
In this population, a higher prevalence
of biliary lithiasis as etiology (68%) of acute
pancreatitis was noted. In the last 12 years,
overweight and obesity, directly related to
formation of biliary stones, have reached
71.3% in the adult population, an increase
of almost 10% compared to the year 2000 15.
In our study, the presence of ΔCl>
8mEq/L was an important predictor for
hospital stay, even better than the APACHE
II scale at admission and at 24 hours, only
comparable with severity due to Atlanta clas-
sification in acute pancreatitis, even when it
was adjusted in multivariate analysis.
We are aware that our study has limi-
tations, mainly the lack of measurement of
other electrolytes, acid-base and inflamma-
tory balance parameters, such as sodium,
potassium, calcium, magnesium, serum pH,
bicarbonate (HCO3) and C-reactive protein
(CRP), even though several of these elements
are routinely measured in this pathology.
Finally, the type of solution (Hartmann
vs saline solution 0.9%), as well as the vol-
ume of liters used, should be evaluated in
prospective controlled studies given its po-
tential therapeutic effect and prognosis on
days of hospital stay.
We conclude that changes greater than
8mEq/L of chloremia at 24 hours after ad-
mission identifies a subset of patients with
acute pancreatitis with an increased risk of
lengthening their hospital stay and probably
mortality and complications, independently
of other prognostic factors, such as APACHE
II. Hyperchloremia remains a factor of poor
prognosis, highly controllable with adequate
fluid management, as well as being an eas-
ily measurable laboratory parameter that
can better predict an increased probability
of longer hospital stay in adult patients with
acute pancreatitis.
Chloremia changes due to hydric reanimation and complications in pancreatitis 145
Vol. 63(2): 137 - 146, 2022
Funding
The author(s) received no financial
support for the research, authorship, and/or
publication of this article.
Declaration of Conflicting Interests
The author(s) declared no potential
conflicts of interest with respect to the re-
search, authorship, and/or publication of
this article.
Author’s ORCID numbers
• Rafael Silva Olvera (RSO):
0000-0002-3895-1149
• Mauricio Pierdant Pérez (MPP):
0000-0002-4606-0071
• Gustavo Ibarra Cabañas (GIC):
0000-0002-5319-4879
• Iván Ledezma Bautista (ILB):
0000-0003-4747-1777
• Raúl Alejandro Hernández Rocha
(RAHR): 0000-0002-2395-1736
• Antonio Augusto Gordillo Moscoso
(AAGM): 0000-0002-7351-4614
Authors participation
• RSO: participation in the design of
the study, data acquisition final approv-
al of the manuscript.
• MPP: participation in the design of
the study, data analysis, writing of the
manuscript, critical intellectual review,
final approval of the manuscript.
• GIC: data acquisition, data analysis.
• ILB: data analysis, critical intellec-
tual review, final approval of the manu-
script.
• RAHR: writing of the manuscript,
critical intellectual review, final approv-
al of the manuscript.
• AAGM: data analysis, critical intel-
lectual review final approval of the man-
uscript.
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